Aquatic Invasions (2014) Volume 9, Issue 2: 175–182 doi: http://dx.doi.org/10.3391/ai.2014.9.2.06 Open Access

© 2014 The Author(s). Journal compilation © 2014 REABIC

Research Article

Status of the Pacific Oyster Crassostrea gigas (Thunberg, 1793) in the western , – Five years of population development

Tilde Groslier1, Helle Toft Christensen1,2, Jens Davids1, Per Dolmer2,3, Ingrid Elmedal1,4, Mark Wejlemann Holm1 and Benni W. Hansen1* 1Department of Environmental, Social and Spatial Change, Roskilde University, Universitetsvej 1, DK-4000, Denmark 2Technical University of Denmark, National Institute of Aquatic Resources, Jægersborg Allé 1, DK-2920 Charlottenlund, Denmark 3ORBICON A/S Ringstedvej 20, DK-4000, Denmark 4Ecolabelling Denmark, Danish Standards Foundation, Kollegievej 6, DK-2920 Charlottenlund, Denmark *Corresponding author E-mail: [email protected]

Received: 23 September 2013 / Accepted: 3 April 2014 / Published online: 15 April 2014 Handling editor: Phipppe Goulletquer

Abstract

The Pacific oyster, Crassostrea gigas, was introduced into the Netherlands in 1964 for aquaculture purposes and has since spread extensively in Northern European waters. Eight locations in the western part of the Limfjord, Denmark, first sampled in 2006 were revisited in 2011, to determine how the population of C. gigas has changed. Densities were lower at all but two locations. No differences in average shell lengths or condition indices were detected. No changes in the number or distribution of shell size classes were observed. These similarities suggest there is a single population that has not expanded in terms of geographic distribution. While reproduction does occur, conditions for population growth appear to be suboptimal. The species has become established in western Limfjord but abundance is low and densities are much lower than those considered harmful to the ecosystem. At present, the C. gigas population is not a cause for concern in the Limfjord ecosystem. Key words: invasive bivalve, winter mortality, abundance, population development, distribution

Introduction early 1980s, extensive spat falls were observed (Drinkwaard 1999). The Pacific Oyster Crassostrea gigas (Thunberg, Warm summers and mild winters may have 1793) is native to Japan and the Pacific Coasts of aided the dispersal of C. gigas in northern Europe Asia between latitudes ~30°N and ~48°N (Arakawa (Nehls et al. 2006; Troost 2010). Furthermore, a 1990). Crassostrea gigas was first introduced to lack of predators and a high competitive ability Europe as a bivalve aquaculture species in 1964 have contributed to the establishment of this due to a severe decline in the populations of the invasive bivalve (Nehls et al. 2006; Schmidt et native European oyster Ostrea edulis Linneaus, al. 2008; Troost, 2010). 1758 (Shatkin et al. 1997; Reise et al. 1999). Spat In the Limfjord, Denmark, C. gigas was of C. gigas was first imported to the Oosterschelde, introduced in 1972 for aquaculture purposes but The Netherlands, from British Columbia, Canada, culture efforts have since been abandoned and a successful trial to grow the species commer- (Jensen and Knudsen 2005). In coastal systems, cially was carried out (Drinkwaard 1999). The low it is nearly impossible to control an ongoing water temperatures in the Oosterschelde estuary invasion regardless of whether the non-native were deemed to be unfavorable for reproduction; species is benign or has a negative impact on the thus, subsequent import for aquaculture was system (Reise et al. 2006). C. gigas has established allowed (Shatkin et al. 1997; Drinkwaard 1999; reproducing populations in Scandinavia (Wrange Wehrmann et al. 2000). However, C. gigas did et al. 2010), and there is concern that the reproduce in the Dutch estuaries and, by the dispersal of C. gigas in the Limfjord may have a

175 T. Groslier et al. negative impact on populations of the native blue shoreline 20 m apart. The starting point was the mussel Mytilus edulis Linnaeus, 1958 and high water mark, which was marked by bands of presumably also on Ostrea edulis; both represent deposited seaweed. GPS positions were recorded important fisheries resources in the estuary at start and end of each transect line, and water (Dolmer and Frandsen 2002; Wrange et al. 2010). depth was measured in 5 m intervals along the A population survey of C. gigas was conducted line. Sampling at water depths below 0.6 m was at eight locations in the western part of the done in waders with aquascopes (Strand et al. Limfjord during the summer (late July – late 2012). At depths between 0.6 and 1 m, sampling September) of 2006, and sampling was repeated was done by SCUBA divers. At Agger Tange, during June - August 2011 to determine how the Rønland, Lysen Bredning and Vile Vig, the population had changed. Specifically, we compared sampling in 2011 was done to a depth of 0.6 m. estimates of abundance, shell size, and condition At Klosterbugten, Harrevig, Hjortholm and between the two sampling periods. Dråby Vig, three of the five transects were done to a depth of 1.0 m (Table 1). At locations where Methods three long and two short transects were made; the average length refers to the three long Study area transect lines. Rønland in 2006 was not surveyed The Limfjord is a long and shallow sound that by transect, and no attempt to collect individuals separates the northern part of from the for calculating densities was done. Some specimens mainland; it is approximately 170 km long with a were collected to determine condition from this site. 1,000 km coastline, and an average depth of 4.3 Every C. gigas found within 1 meter on either m (Naturstyrelsen 2009; Miljøcenter Aalborg 2007). side of the transect line was collected and shell The system is connected to the in the length (SL) and distance from shore were west and to the in the east (Figure 1). recorded. Only individuals > 50 mm SL were An easterly current, combined with fresh-water included to minimize detection bias. Living inputs from the surrounding catchment area, individuals were retained for further processing results in a highly saline environment (salinity and dead individuals were discarded. The shell 32) in the westerly part of the sound, where the length of dead individuals was measured in 2011 North Sea water enters the system at Thyborøn only. To be included, the left and right valves Channel, and a lower salinity (salinity 18) in the had to be connected, indicating a recent death eastern part of the sound (Dolmer 2000; (1–2 years). No consideration was given to the Miljøcenter Aalborg 2007). The current patterns extent of epiphytic growth on empty shells. have not changed significantly since 1875 In 2011, the south eastern coast of Fur (Figure (Naturstyrelsen 2009). 1) was searched for C. gigas. This was done with Water temperatures range from 2–3°C in winter waders and aquascope at five sites along the to 15–17°C in summer (Wiles et al. 2006). shoreline. Locations were chosen based on Limfjorden is considered a eutrophic system due availability, and 20–30 m of the sea floor along to high nutrient loading from the surrounding the coast was randomly scanned to a water depth catchment area. Parts of the sound are subject to of approximately 1 m. recurring oxygen depletions, although there are Each living C. gigas retained was provided large inter-annual differences in duration and the with a unique number, placed in individual bags, area affected (Dolmer et al. 2009). The annual and stored frozen at -18 °C before further treatment. primary production in the western part of the After thawing, the shell length was measured, Limfjord is approximately 90–100g C m-2 and the flesh and shell was separated. The flesh (Limfjordsovervågningen 2005). was dried at 105°C until constant shell-free dry weight (SFDW) was reached. Shells were washed Sample collection and cleaned, then dried until they reached constant weight (Shell DW). Eight locations (Table 1) in the western part of Condition (C) for each individual was the Limfjord were surveyed in 2006 and 2011 calculated as: (Figure 1). An additional station, Fur, was added in 2011 to determine whether C. gigas had spread C = (SFDW/SDW) × 1,000 further east in the estuary. At each location, five transect lines (four at for shell free dry weight (SFDW in g) and shell Hjortholm) were placed perpendicular to the dry weight (SDW in g) (Brown and Hartwick 1988;

176 Status of Crassostrea gigas in the western Limfjord, Denmark

Figure 1. Overview of the study area in the western part of the Limfjord. Dråby Vig, Klosterbugten, Harrevig, Lysen Bredning, Vile Vig, Hjortholm, Agger Tange, Rønland, Fur. Solid circles mark presence in both years, open circle means not found in 2011 and not sampled in 2006, open square means found in 2011 and not sampled in 2006, and the solid square means found in 2006 and not found in 2011. Red circles show locations of anecdotal reports of C. gigas.

Table 1. All sampled locations presented with regional designations. Corresponding coordinates for the start point of the first transect at each location are noted, as are the average transect length, and the water depth at the end of transect. Coordinates for Fur designate the first site of survey (only in 2011). Number of specimens presents all living C. gigas found along the transect lines at each location. Density averages m-2 for each location are presented with standard deviations. Statistical significance between 2006 and 2011 is marked with an ‘s’ (Mann- Whitney test: p<0.05), non-significance is marked ‘ns’. Arrows mark an increase (up) or decrease (down) in density. Densities are stated for the long transects where those were applied in 2011. No density data were collected for Rønland in 2006 or for Fur.

Avg. -2 Coordinates Water No. specimens Density (m ) transect Signi- Location depth length ficance (m) Lat Long ± sd (m) 2006 2011 2006 2011

Klosterbugten, Mors 56.791634 8.860580 128.0 ± 7.6 1.0 52 153 0.02±0.04 0.12±0.12 ns ↑ Dråby Vig, Mors 56.868258 8.828974 258.0 ± 2.9 1.0 78 94 0.04±0.01 0.06±0.01 ns ↑ Harrevig, Salling 56.709785 8.897354 187.0 ± 7.6 1.0 67 28 0.18±0.04 0.02±0.02 ns ↓

Lysen Bredning, Salling 56.686789 8.840281 47.0 ± 3.0 0.6 35 1 0.02±0.02 0.004±0.01 ns ↓

Vile Vig, Salling 56.710474 8.866136 26.0 ± 4.2 0.6 30 0 0.06±0.06 0.00±0.00 ns ↓

Hjortholm, Salling 56.696486 8.846435 82.0 ± 12.6 1.0 52 1 0.04±0.02 0.002±0.04 ns ↓

Agger Tange, Thyborøn 56.722358 8.251669 10.0 ± 1.9 0.6 47 20 3.12±1.37 0.20±0.13 s ↓

Rønland, Thyborøn 56.672144 8.213861 83.0 ± 5.3 0.6 n.a. 38 n/a 0.04±0.06 - -

S-E coast of Fur 56.805729 9.022294 n.a. n.a. n.a. 0 n/a n/a - -

177 T. Groslier et al.

Statistical analyses

All statistical analyses were performed using GraphPad Prism 5 software (GraphPad Software, California). Level of significance was α = 0.05 for all tests. Abundances were compared with a two- way ANOVA test, followed by Sidak's multiple comparisons test. Abundance data were transformed using square-root (x + 0.5). Shell lengths and condition data were analysed through two-way ANOVAs and Sidaks’s multiple comparisons tests. Differences between shell-length frequencies between years and between winter and summer 2011 were detected by means of Kolmogorov- Smirnov tests. Modes, assumed to correspond to cohorts or age classes, were determined using Bhattacharya’s Method in the FiSAT II software (FAO, Rome). This method visually separates normally distributed groups from a mixed group, by using natural logarithms on ratios of frequencies, overlapping distributions can be identified (Goonetilleke and Sivasubramaniam 1987).

Results

The analysis showed that the interaction term, the year, and the location had significant effects on abundance of C. gigas (Table 2A). Overall, the abundance C. gigas declined between 2006 and 2011, with Agger Tange having the highest decline in abundance (Table 1). For the average shell lengths (± SD), only the interaction term and the location were significant (Table 2B). Between the years, there was a significant difference seen at Dråby Vig, Harrevig, Klosterbugten, Agger Tange, and Rønland, but these were not consistent. The shell lengths at Dråby Vig, Klosterbugten, and Agger Tange decreased between 2006 and 2011; while at Harrevig and Rønland, shell length has increased (Figure 2A). The average condition (± SD) of C. gigas Figure 2. A: Average shell lengths ± SD for each location. Star showed significant effects of the interaction denotes a significant difference. B: Average condition ± SD for term, the year, and the site (Table 2C). The only each location. Star denotes a significant difference. significantly different locations were Dråby Vig and Harrevig, which both show decreased condition from 2006 to 2011 (Figure 2B). No specimens were found at Vile Vig or Lysen Crosby and Gale 1990). This method was chosen Bredning in 2011. because of its ease of measurement, and it is the Based on Kolmogorov-Smirnov tests, the shell most relevant index for examining the physio- length-frequencies between 2006 and 2011 were logical state of the oyster (Lucas and Beninger significantly different (p ≤ 0.01), with more 1985; Brown and Hartwick 1988). small animals collected in 2006 (Figure 3).

178 Status of Crassostrea gigas in the western Limfjord, Denmark

Discussion 14 A By revisiting the same sampling stations after 12 five years, it is clear that C. gigas remains present 10 in the western part of the Limfjord; however, 8 abundance has decreased at most locations. The stochastic nature of the changes in population 6 densities suggests physical conditions (e.g., 4 Frequency (%) salinity) may be limiting the dispersal of C. 2 gigas in the Limfjord. It may well be that C. gigas has not had enough time to have been able 0 50 75 100 125 150 175 200 225 250 to establish colonies further east than Mors. If this is the case, regular visits to the east of the Shell length (mm) study area will be of great value in determining 14 B the long term dispersal rate of which the oyster 12 is moving through the Limfjorden ecosystem. The two winters preceding 2011 were harsh, 10 with average air temperatures of -1.5°C and -1.3°C 8 in 2009–2010 and 2010–2011, respectively (with 6 a normal 30-year average of 0.5°C (DMI 2010; DMI 2011)). Crassostrea gigas generally occurs

Frequency (%) 4 in areas with a sea surface temperature between - 2 1.9°C and 19.8°C in the coldest month of the 0 year (Carrasco and Barón 2010). Few live 50 75 100 125 150 175 200 225 250 specimens were collected in the shallow water Shell length (mm) close to the shore, and the size frequency analysis shows that the dead specimens tend to be larger 14 C than the live oysters. Crassostrea gigas has been 12 shown to have a decreased mortality with increased 10 water depth in Scandinavia, which may well explain the observed pattern (Strand et al. 2012). 8 The specimens located in shallow waters would 6 be exposed to the mechanical stress caused by

4 ice, as well as the cold air temperatures.

Frequency (%) Frequency Mortalities during the winters 2009/10 and 2010/11 2 at Agger Tange were found to be 17% and 13%, 0 respectively (MW Holm, unpublished data). 50 75 100 125 150 175 200 225 250 Predators or wave action potentially can remove Shell length (mm) shells, and result in some uncertainty and Figure 3. The number of cohorts and their size vs. frequency underestimations in the data. Reports of mortalities distribution, of the collected C. gigas: total live 2006 (A), total during harsh winters from the Wadden Sea are live 2011 (B), and total dead 2011 (C). Data for mean lengths, much higher than found at Agger Tange; with standard deviations, and number of individuals in the groups is mortalities ranging from 34 to 90% (Reise 1998; shown in Table 3. Büttger et al. 2011). The Limfjord seems to be a more protected environment, which could be due to the protection land-fast ice would afford, and although the harsh winters have an effect, it seems Overwinter mortality in 2011 was highly size not to be a major regulator of the population. selective (P < 0.01) with large animals (>125 mm Dredging samples in the Limfjord have revealed SL) largely disappearing from the population. few to no specimens in waters > 3 m deep (P In 2006, three apparent cohorts were observed Dolmer, unpublished data), although the species in living animals, while in 2011 (living animals) has been observed at depths > 40 m deep only one cohort could be identified. There were elsewhere (Minchin and Gollasch 2008). Thus two clear modes in the length distribution of the species has yet to spread to the deeper waters dead animals collected in 2011 (Table 3, Figure 3). of the Limfjord. All locations are accessible to

179 T. Groslier et al.

Table 2. ANOVA tables for A) Abundance, B) Shell lengths, and C) Condition.

SS DF MS F (DFn, DFd) P value A Interaction 2.104 6 0.3507 F (6, 56) = 34.10 P < 0.0001 Site 3.548 6 0.5914 F (6, 56) = 57.51 P < 0.0001 Year 0.4360 1 0.4360 F (1, 56) = 42.40 P < 0.0001 Residual 0.5758 56 0.01028 B Interaction 66025 7 9432 F (7, 826) = 25.29 P < 0.0001 Site 74899 7 10700 F (7, 826) = 28.69 P < 0.0001 Year 364.0 1 364.0 F (1, 826) = 0.9760 P = 0.3235 Residual 308056 826 372.9 C Interaction 76112 7 10873 F (7, 572) = 14.76 P < 0.0001 Site 22284 7 3183 F (7, 572) = 4.320 P = 0.0001 Year 18437 1 18437 F (1, 572) = 25.02 P < 0.0001 Residual 421470 572 736.8

Table 3. Data for the total and the regionally grouped cohort analysis, using Bhattacharya’s Method in the FiSAT II software. Shown are the numbers of age groups in each year, the mean length of each group, standard deviation, number of individuals belonging to each group, and the Separation Index (S.I.). A S.I. > 2 indicates a reliable separation of the size classes. No dead specimens were collected in 2006.

A Total live 2006 Total live 2011 Size Mean (mm) SD Individuals S.I. Mean (mm) SD Individuals S.I. group 1 55.1 9.9 264 n.a. 86.8 19.2 330 n.a. 2 92.3 11.8 201 3.44 - - - - 3 124.8 11.1 45 2.84 - - - - B Total dead 2006 Total dead 2011 Size Mean (mm) SD Individuals S.I. Mean (mm) SD Individuals S.I. group 1 n.a. n.a. n.a. n.a. 69.5 10.6 45 n.a. 2 n.a. n.a. n.a. n.a. 120.1 15.0 163 3.95

larvae that are carried with the currents, sometimes frequent storms) can greatly reduce the population for weeks, before they settle as spat (Quale 1988; size, and result in a temporary setback for local Wehrmann et al. 2000). The transport of larvae populations; however, but the high fecundity of from one location to the others likely takes C. gigas gives the population high potential for place, probably through a stepping stone process. expansion during warm summers (Büttger et al. Reproduction at Agger Tange was detected in 2011). Locations like Fur, where no C. gigas 2004, 2007 and 2008, and spawning oysters were were found, could easily be populated by spawn observed when sampled for this study (MW released at near-by locations. Holm, unpubl. data). However, the rate at which That the Pacific oyster is still in the establish- the settled larvae mature into reproducing indi- ment phase (sensu Reise et al. 2006) in the viduals is currently unknown. Since reproduction Limfjord is a hypothesis supported by the pattern appear to be continuous, and under the proper between sites, years, and interaction terms seen environmental circumstances can result in a in the data, and relatively low numbers of small massive settlement of juvenile oysters, monitoring specimens in 2011. In the Limfjord, the species of the recruitment would appear to be warranted. is subjected to colder water temperatures and a Winters with heavy ice formation (and perhaps different environment than its natural habitat,

180 Status of Crassostrea gigas in the western Limfjord, Denmark and has not yet fully adapted to conditions in the Carrasco MF, Barón PJ (2010) Analysis of the potential Limfjord ecosystem. However, C. gigas is not geographic range of the Pacific oyster Crassostrea gigas (Thunberg, 1793) based on surface seawater temperature situated at its northernmost limit in Denmark, as it satellite data and climate charts: the coast of South America is reproducing and settling successfully in as a study case. Biological Invasions 12: 2597–2607, Norway and Sweden (Wrange et al. 2010). The http://dx.doi.org/10.1007/s10530-009-9668-0 density data shows that the abundance is very Crosby MP, Gale LD (1990) A review and evaluation of bivalve 2 condition index methodologies with a suggested standard low, with less than one specimen per m , yet method. Journal of Shellfish Research 9 (1): 233–237 spawning individuals were observed in 2011 at Diederich S (2006) High survival and growth rates of introduced both sampling times, and during the sampling in pacific oysters may cause restrictions on habitat use by native mussels in the Wadden Sea. Journal of Experimental Marine 2006. The species has so far failed to become Biology and Ecology 328: 211–227, http://dx.doi.org/10.1016/j. truly invasive, i.e., a threat to the Limfjord. jembe.2005.07.012 Nevertheless, it has successfully colonized the DMI (2010) The Danish Meteorological Institute: http://www.dmi. dk/dmi/vejret_i_danmark_-_vinteren_2009-2010 Limfjord, albeit at low abundance. Several mild DMI (2011) The Danish Meteorological Institute: http://www.dmi. winters accompanied by warm summers could dk/dmi/vejret_i_danmark___vinteren_2010-2011 change this state. A combination of large Dolmer P (2000) Algal concentration profiles above mussel beds. Journal of Sea Research 43: 113–119, http://dx.doi.org/10.1016/ reproduction events; ideal conditions for settlement, S1385-1101(00)00005-8 recruitment, and growth; and several years with Dolmer P, Frandsen RP (2002) Evaluation of the Danish mussel low overwinter mortalities could trigger a rapid fishery: Suggestions for an ecosystem management approach. population expansion. The main limitation for Helgoland Marine Research 56: 13–20, http://dx.doi.org/10. 1007/s10152-001-0095-6 the spread of C. gigas, however, is unlikely to be Dolmer P, Kristensen PS, Hoffmann E, Geitner K, Borgstrøm R, only due to climatic conditions. It has been Espersen A, Petersen JK, Clausen P, Bassompierre M, present in the Limfjord for 40 years without Josefson A, Laursen K, Petersen IK, Tørring D, Gramkow M experiencing the same expansion and growth that (2009) Udvikling af kulturbanker til produktion af blåmuslinger i Limfjorden. DTU Aqua-rapport nr. 212–2009. has been seen in the Wadden Sea. This difference Charlottenlund. Institut for Akvatiske Ressourcer, Danmarks in success may be linked to the tidal effects: tidal Tekniske Universitet, 127 pp range in the Limfjord is about 0.2 m compared to Drinkwaard AC (1999) Introductions and developments of oysters 2 m in the Wadden Sea (Dolmer and Frandsen in the North Sea area: a review. HelgoländerMeeresunters 52: 301–308, http://dx.doi.org/10.1016/0044-8486(85)90243-1 2002; Diederich 2006). Thus, at the shallow-water Goonetilleke H, Sivasubramaniam K (1987) Separating Mixtures Limfjord stations, the supply of phytoplankton of Normal Distributions: Basic Programs for Bhattacharya’s typically replenished (presumably from offshore) Method and their Applications to Fish Population Analysis. by tidal mixing and transport may be reduced, Marine Fishery Resources Management in the Bay of Bengal, Food and Agriculture Organization of the United Nations resulting in localized food limitation. Jensen KR, Knudsen J (2005) A summary of alien marine benthic invertebrates in Danish waters. Oceanological and Hydrobiological Studies 34 (Suppl. 1): 137–162 Acknowledgements Limfjordsovervågningen (2005) NOVANA – Vandmiljø i Lim- fjorden 2004. Ringkøbing, Viborg and Nordjyllands Amter We are indebted to KL Johnsen (RUC), A Groslier and H Lucas A, Beninger PG (1985) The use of physiological condition Heidemann for aiding in the field, A Faarborg (RUC) for help and indices in marine bivalve aquaculture. Aquaculture 44: 187– guidance in the laboratory, and Å Strand (University of 200, http://dx.doi.org/10.1016/0044-8486(85)90243-1 Gothenburg) for providing access to unpublished articles. We Miljøcenter Allborg (2007) Fakta om Limfjorden http://www. thank two anonymous reviewers and JM Hanson for constructive limfjord.dk/om_fjord.htm (Accessed 10 January 2012) criticism of earlier versions of the manuscript and to D Hoff for Minchin D, Gollasch S (2008) Crassostrea gigas. Delivering help with English usage. This work was supported by the Danish Alien Invasive Species Inventories for Europe (DAISIE). Scientific Council for Independent Research, Natural Sciences, http://www.europe-aliens.org (Accessed 20 March 2012) MARINVA proj. no. 09-066004. Naturstyrelsen (2009) http://www.naturstyrelsen.dk/Vandet/Havet/Dan skeFarvande/Limfjorden/Fakta_om_Limfjorden.htm (Accessed 20 References March 2012) Nehls G, Diederich S, Thieltges DW, Strasser M (2006) Wadden Arakawa KY (1990) Commercially important species of oysters Sea mussel beds invaded by oysters and slipper limpets: in the world. Marine Behaviour and Physiology 17: 1–13, competition or climate control? Helgoland Marine Research http://dx.doi.org/10.1080/10236249009378756 60: 135–143, http://dx.doi.org/10.1007/s10152-006-0032-9 Brown JR, Hartwick EB (1988) Influences of Temperature, Quale DB (1988) Pacific Oyster Culture in British Columbia. Salinity and Available Food upon Suspended Culture of the Canadian Bulletin of Fisheries and Aquatic Sciences 218, 241 Pacific Oyster, Crassostrea gigas – II. Condition and pp Survival. Aquaculture 70: 253–267, http://dx.doi.org/10.1016/ Reise K (1998) Pacific oysters invade mussel beds in the 0044-8486(88)90100-7 European Wadden Sea. Senckenbergiana maritima 28: 167– Büttger H, Nehls G, Witte S (2011) High mortality of Pacific 175, http://dx.doi.org/10.1007/BF03043147 oysters in a cold winter in the North-Frisian Wadden Sea. Reise K, Gollasch S, Wolff WJ (1999) Introduced marine species Helgoland Marine Research 65: 525–532, http://dx.doi.org/10. of the North Sea coasts. Helgoländer Meeresunters 52: 219– 1007/s10152-011-0272-1 234, http://dx.doi.org/10.1007/BF02908898

181 T. Groslier et al.

Reise K, Olenin S, Thieltges DW (2006) Are aliens threatening Troost K (2010) Causes and effects of a highly successful marine European aquatic coastal ecosystems? Helgoland Marine invasion: Case-study of the introduced Pacific oyster Research 60: 77–83, http://dx.doi.org/10.1007/s10152-006-0024-9 Crassostrea gigas in continental NW European estuaries. Schmidt A, Wehrmann A, Dittmann S (2008) Population Journal of Sea Research 64: 145–165, http://dx.doi.org/10. dynamics of the invasive Pacific oyster Crassostrea gigas 1016/j.seares.2010.02.004 during the early stages of an outbreak in the Wadden Sea Wehrmann A, Herlyn M, Bungenstock F, Hertweck G, Millat G (Germany). Helgoland Marine Research 62: 367–376, (2000) The Distribution Gap is Closed – First Record of http://dx.doi.org/10.1007/s10152-008-0125-8 Naturally Settled Pacific Oysters Crassostrea gigas in the Shatkin G, Shumway SE, Hawes R (1997) Considerations East Frisian Wadden Sea, North Sea. Senckenbergiana regarding the possible introduction of the Pacific oyster maritima 30: 153–160, http://dx.doi.org/10.1007/BF03042964 (Crassostrea gigas) to the Gulf of Maine: A review of global Wiles PJ, van Duren LA, Häse C, Larsen J, Simpson JH (2006) experience. Journal of Shellfish Research 16(2): 463–477 Stratification and mixing in the Limfjorden in relation to Strand Å, Blanda E, Bodvin T, Davids JK, Jensen LF, Holm- mussel culture. Journal of Marine Systems 60: 129–143, Hansen TH, Jelmert A, Lindegarth S, Mortensen S, Moy FE, http://dx.doi.org/10.1016/j.jmarsys.2005.09.009 Nielsen P, Norling P, Nyberg C, Christensen HT, Vismann B, Wrange A-L, Valero J, Harkestad LS, Strand Ø, Lindegarth S, Wejlemann Holm M, Winding Hansen B, Dolmer P (2012) Christensen HT, Dolmer P, Kristensen PS, Mortensen S Impact of an icy winter on the Pacific oyster (Crassostrea (2010) Massive settlement of the Pacific oyster, Crassostrea gigas Thunberg, 1793) populations in Scandinavia. Aquatic gigas, in Scandinavia. Biological Invasions 12: 1145–1152, Invasions 7: 433–440, http://dx.doi.org/10.3391/ai.2012.7.3.014 http://dx.doi.org/10.1007/s10530-009-9535-z

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